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Temperature Influences the Activity Patterns of Armadillo Species in a Large Neotropical Wetland

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Temperature Influences the Activity Patterns of Armadillo Species in a Large Neotropical Wetland Mamm Res DOI 10.1007/s13364-015-0232-2 ORIGINAL PAPER Temperature influences the activity patterns of armadillo species in a large neotropical wetland Thiago Bernardes Maccarini1 & Nina Attias1 & Ísis Meri Medri2 & Jader Marinho-Filho3 & Guilherme Mourão4 Received: 30 October 2014 /Accepted: 14 June 2015 # Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2015 Abstract In this study, we characterized the activity patterns short period in the middle of the morning and/or afternoon. and estimated the activity overlap between two armadillo spe- The proportion of activity overlap was 0.28 between the spe- cies (Dasypus novemcinctus and Euphractus sexcinctus)in cies, occurring primarily at the beginning of the night. At the Pantanal wetlands of Brazil. We report the effect of daily lower temperatures, yellow armadillos tended to leave their mean ambient temperature on activity onset and duration of burrows earlier and were active for longer periods. This is these armadillos. We captured seven yellow armadillos and probably an adaptation to their physiological constraints and three nine-banded armadillos and fitted them with very high limited thermoregulatory capabilities. Xenarthrans could be frequency radios and temperature loggers. By monitoring the used as models to obtain valuable information about how temperature of the environment (air temperatures and burrow physiology affects mammal behavior. temperatures), we inferred when the armadillo was active (above ground) or inactive (inside the burrow). Yellow arma- Keywords Thermoregulation . Euphractus sexcinctus . dillos were active mainly during the daytime and in the begin- Dasypus novemcinctus . Burrow . Niche partitioning . ning of the night, while nine-banded armadillos were active Physiological constraints mainly during the night. However, nine-banded armadillos presented a bimodal activity pattern, becoming active for a Introduction Communicated by: Karol Zub The circadian activity period adopted by an animal is one of Electronic supplementary material The online version of this article the most effective and generalized ways to minimize the in- (doi:10.1007/s13364-015-0232-2) contains supplementary material, fluence of unfavorable biotic and abiotic factors (Layne and which is available to authorized users. Glover 1985). Circadian activity cycles allow an animal to anticipate environmental changes and choose the appropriate * Nina Attias [email protected] moment for a specific response or activity (Aronson et al. 1993). Most armadillos (Mammalia: Cingulata) have a strategy for 1 Ecology and Conservation Graduate Program, Centro de Ciências avoiding unfavorable factors: they build or use burrows. Biológicas e da Saúde - Cidade Universitária, Federal University of Mato Grosso do Sul, s/n - Caixa Postal 549, Campo Grande, MS, Burrows can be used not only to escape from predators or Brazil for sleeping (McDonough and Loughry 2003; Desbiez and 2 Ecology Graduate Program, Centro de Ciências Biológicas e da Kluyber 2013) but also for thermoregulation (González et al. Saúde - Cidade Universitária, University of Brasilia, s/n - Caixa 2001). Burrows work as temperature buffers (González et al. Postal 549, Campo Grande, MS, Brazil 2001); armadillos can exit them once air temperatures are 3 Zoology Department, University of Brasilia, Campus Universitário favorable and return to them to maximize their energy Darcy Ribeiro, Brasília, DF, Brazil budgets. 4 Embrapa Pantanal, Brazilian Agricultural Research Corporation, Rua Mammalian circadian rhythms are responsive to environ- 21 de Setembro 1880, Corumbá, MS, Brazil mental factors, especially light cycles (Aronson et al. 1993). Mamm Res However, armadillos are imperfect homeotherms and have McDonough 2013). Hence, the available ecological informa- limited thermoregulatory capabilities, low body temperatures, tion might not reflect patterns that can change from place to and low basal rates of metabolism (McNab 1985). These char- place, such as behavior. acteristics are probably associated with their burrowing activ- Therefore, the purpose of this study was to characterize the ity and feeding habits (McNab 1979, 1980). As a result of this activity patterns of these two species of armadillo in the unique characteristic among mammals, air temperature Brazilian Pantanal, estimate their activity overlap, and deter- strongly affects the activity patterns of armadillos and other mine the influence of air temperature on their activity patterns. xenarthrans (Layne and Glover 1985; Chiarello 1998;Mourão and Medri 2007). The influence of temperature on the activity patterns of these animals can be determined from their activity Methods duration and timing (activity onset). Temporal niche partitioning is a mechanism that related Study area species adopt to avoid competition: different circadian activity patterns might result in differentiation of the use of resources The Pantanal is a large wetland region covering approximately or levels of predation susceptibility. It can facilitate coexis- 210,000 km2 of seasonal floodplain of Rio Paraguay and in- tence through avoidance of direct confrontation (interference cludes areas of Brazil, Bolivia, and Paraguay (Mittermeier competition) or through the reduction of overlap in resource et al. 2003). The Brazilian portion of Pantanal is located in demand (resource competition; Kronfeld-Schor and Dayan the western part of the country, near the geographic center of 2003). Partitioning of the temporal dimension of the niche South America, at about 100 m in elevation. We conducted between two species implies a smaller niche overlap than ex- our study at the Nhumirim Ranch (18°59′ S, 56°39′ W), an pected by chance. In this phenomenon, the less competitive experimental station of approximately 43 km2 located in the species, or subordinates, usually modify their activity to sub- Nhecolândia subregion in the state of Mato Grosso do Sul, optimal periods of the circadian cycle, reducing competition Brazil. The Nhecolândia subregion is characterized by a land- with the dominant species (Gutman and Dayan 2005). scape mosaic of savannas, scrub savannas, forests, and per- However, when competition is not the most important factor, manent and temporary ponds (Alho et al. 1987). the activity periods of similar species can tolerate an overlap The climate of the region is tropical semi-humid, and the higher than that expected by chance. This pattern might indi- average annual temperature is 25.5 °C (Calheiros and Fonseca cate that the activity periods of both species are influenced by 1996). Summers are hot and rainy, averaging 1100 mm rain- similar responses to external factors (e.g., external temperature fall and maximum air temperatures exceeding 40 °C. Winters or potential predators). Another hypothesis is that phylogenet- are warm and dry, averaging less than 300 mm rainfall and air ic constraints of the activity period make closely related spe- temperatures of 20 °C, though occasional cold fronts from the cies present similar activity patterns, limiting the opportunities south can cause air temperatures as low as 0 °C (Soriano et al. for temporal niche partitioning among closely related compet- 1997). itors (Roll et al. 2006). Even though there is no evidence to confirm this fact, this could be the case for armadillos given Data collection that their physiology makes them very sensitive to tempera- ture variations. During September 2007 and February–May 2010, we The yellow armadillo, Euphractus sexcinctus (Linnaeus searched for armadillos by foot or in an all-terrain vehicle, 1758), and the nine-banded armadillo, Dasypus novemcinctus catching eight armadillos by hand and two in live traps from (Linnaeus 1758), are sympatric burrowing armadillos that simultaneous studies focused on medium-sized carnivores in have overlapping dietary habits (Anacleto 2007) and may oc- the area. Of these, seven were yellow armadillos cupy the same habitat type in the Brazilian Pantanal. The (E. sexcinctus) and three were nine-banded armadillos former is a diurnal and conspicuous species, widely distribut- (D. novemcinctus). We placed them in a safe and ventilated ed throughout Brazil (except Amazonia) and South America, box and then transported them to the ranch laboratory. They and is very common in the Pantanal (Eisenberg and Redford were anesthetized there using an intramuscular dose of 1999). Despite these characteristics, its ecology is poorly 4 mg/kg Zoletil® (1:1 tiletamine hydrochloride and known, and studies on its activity patterns are rare (Bonato zolazepam hydrochloride; Virbac S.A., Cedex, France). et al. 2008). The latter is a predominantly nocturnal species They were weighed, measured, and marked with numbered (Emmons and Feer 1997; Eisenberg and Redford 1999)thatis ear tags (model 1005-4; National Band & Tag Co., Newport, found from Argentina to the USA, which is considered as the KY, USA). largest geographic range among armadillos (Wetzel 1985). With the animals under anesthesia, we attached a package Even though this is the most studied species, much of the (≈35 g) containing a StowAway Tidbit temperature data log- research has been done in the USA (Loughry and ger (Onset Computer Corporation, Bourne, MA, USA; Mamm Res accuracy, ± 0.4 °C at 20 °C) combined with a very high fre- whether our method was reliable at inferring when the arma- quency radio transmitter (frequency range 164–166 MHz; dillos were inside or outside the burrows, we also performed model R2030; Advanced Telemetry Systems,
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